Acanthocheilus rotundatu

Moravec, F. & Nagasawa, K., 2000, Two remarkable nematodes from sharks in Japan, Journal of Natural History 34 (1), pp. 1-13 : 2-11

Acanthocheilus rotundatu s ( Rudolphi, 1819)

(®gures 1, 2) Ascaris rotundata Rudolphi, 1819; A. bicuspis Wedl, 1855 ; Acanthocheilus quadridentatus

Molin, 1858; A. intermedius Orley È, 1885 ; Anacanthocheilus australis Johnston and

Mawson, 1945.

D escription

Medium-sized nematodes. Cuticle almost smooth; however, near body ends mostly with ®ne transverse striation. Lateral alae absent. Oral opening surrounded by three small lips, each of them with two teeth bearing two large, anteriorly directed points. Inner surface of lips forming distinct longitudinal wrinkles (®gure 2B). Interlabia absent. Dorsal lip bearing two double papillae, each dorsoventral lip one double papilla, one single papilla and amphid. Oesophagus muscular, claviform. Nerve ring encircling oesophagus approximately at one-third to one-quarter of its length. Ventriculus spherical, narrower than oesophagus. Ventricular appendix or intestinal caecum absent. Deirids near level of nerve ring. Tail conical, relatively short.

Male (two specimens from M. griseus ; measurements of two smaller specimens from M. manazo in parentheses). Body 34,134 ±36,277 (21,362±23,587) long, maximum width 845 (515±618). Length of lips 24±28 (16±30), their width 64±80 (70); teeth 12±14 (12) long. Oesophagus 2760 ±2966 (1751) long, its maximum width 412±433 (313±339) (7.6±8.7% [7.4±8.2%] of body length). Nerve ring and excretory pore 705±800 (574±687) and 731±835 (618±722), respectively, from anterior extremity. Ventriculus 305±365 (174±226) long and 357±548 (261±270) wide. Spicules equal, weakly sclerotized, 408±640 (280±324) long, representing 1.2±1.8% (1.3±1.4%). Preanal papillae: 28 ±29 (25 in larger specimen) pairs of small subventral papillae; adanal papillae: two (three in larger specimen) pairs; postanal papillae: six (six) pairs of hardly visible papillae of which fourth pair (phasmids) situated more laterally. Ventral precloacal region of two largest males bearing numerous ®ne longitudinal cuticular ridges (crests) (not visible in smaller specimens from M. manazo ). Tail conical, 124±188 (165) long, with rounded tip.

Female (one gravid specimen from M. griseus ; measurements of one non-gravid specimen from M. manazo in parentheses). Body 61,924 (48,925) long, maximum width 1401 (845). Length of lips 40 (cephalic end damaged), their width 88 (±); teeth 16 (±) long. Oesophagus 3646 (2884) long (5.9% [6.0%] of body length], its maximum width 700 (659). Nerve ring and excretory pore 827 (635) and 957 (±), respectively, from anterior extremity. Ventriculus 435 (330) long and 505 (453) wide. Vulva pre-equatorial (slightly post-equatorial), 21,568 (26,842) from anterior end of body (at 38.8% [54.9%] of body length); vulvar lips not elevated. Vagina muscular, directed posteriorly from vulva. Uterus opposed; ovaries tubular, forming numerous coils; anterior ovary reaching anteriorly approximately to distance of one length of oesophagus posterior to oesophagus length; posterior ovary reaching posteriorly almost to rectum. Uterus ®lled with numerous eggs (without eggs), anteriorly reaching level of vulva. Eggs oval, thin-walled, smooth, non-embryonated; mature eggs (n = 10) measuring 72±76Ö48±52 (±). Tail conical, 474 (412) long, with knob-like tail tip, sometimes provided with minute cuticular spike; pair of small lateral phasmids present near posterior end of tail.

Hosts. Spotted smooth-hound, Mustelus griseus Pietschmann, Japanese name`shirozame’, and M. manazo Bleeker, Japanese name`hoshizame’ ( Triakididae , Carcharhiniformes ).

Site of infection. Stomach.

L ocalities. O Sagara ( M. griseus ) and Yui ( M. manazo ), Suruga Bay, North Paci®c Ocean, Japan (18 April and 9 December 1996).

Comments

The only record of this species in Japan is that by Yamaguti (1941) who reported two males from the stomach of Mustelus griseus from the Sea of Ariake (western Kyushu) and one female from Mustelus manazo from the Sea of Japan; however, because he was unable to make a detailed comparison of his specimens with the original species description, his identi®cation as Acanthocheilus quadridentatus (= A. rotundatu s) was only provisional.

In contrast to our ®ndings, Yamaguti (1941) mentions that each of the three lips`bears two teeth, whose anterior ends may be divided into two or three conical or rudimentary points’; he obseved 30±40 preanal papillae on either side and four to ®ve pairs of postanal papillae, spicules only 270±330 m m long, and he did not mention the presence of ventral precloacal cuticular crests in the male. In our opinion, these di erences are due to a certain intraspeci®c variability (his specimens were smaller than most nematodes of the present material) and inaccuracies in observations. Because Yamaguti’s specimens originated from the same host species as those of the present material, there is no doubt that all these nematodes belonged to the same species. Our ®ndings represent the ®rst record of this parasite from the North Paci®c Ocean, o the eastern coast of Japan.

Acanthocheilus rotundatus is a widely distributed parasite of sharks. It was originally described by Rudolphi (1819) from Galeorhinus galeus (Linnaeus) from the Adriatic Sea and later it was reported from di erent species of sharks ( Hexanchus griseus [Bonnaterre], Mustelus antarcticus GuÈnther , M. griseus Pietschmann , M. manazo Bleeker , M. mustelus [Linnaeus], Prionacea glauca [Linnaeus], Scyliorhinus stellaris [Linnaeus], Somniosus microcephalus [Bloch and Schneider]) from Europe, Australia and Japan (e.g. Molin, 1858; Oerly È, 1885; Baylis, 1929; Yamaguti, 1941; Johnston and Mawson, 1943; Hartwich, 1975; Bruce and Cannon, 1990; Petter et al., 1991; Bruce et al., 1994).

The most complete description of A. rotundatus was given by Petter et al. (1991), based on material originating from M. mustelus from the Adriatic Sea. Specimens of the present material from Japan are morphologically very similar to those described by Petter et al. (1991), di ering in somewhat less numerous pairs of preanal papillae (25±29 vs 30±36); Bruce and Cannon (1990) reported even 47 pairs of preanal papillae in A. rotundatus from Australia. However, the number of preanal papillae is subject to a considerable degree of intraspeci®c variability in ascaridoids and, therefore, we consider specimens of the present material to be A. rotundatus . The cephalic structure of this species has been studied by SEM for the ®rst time.

Metaleptus rabuka Machida, Ogawa and Okiyama, 1982 (®gures 3±5)

D escription

Medium-sized nematodes with thin, almost smooth cuticle in smaller specimens and with irregularly transversely striated cuticle in larger specimens. Body of ®xed specimens brown, with dark intestine showing through its posterior part. Cephalic end rounded, formed by two large, massive lateral pseudolabia with bases not separated from body. Inner surface of pseudolabia trilobed in apical view, each lobe bearing small tooth, consisting of three sclerotized pieces, one larger in middle and one smaller on either side; middle lobe and its teeth somewhat larger than both submedian lobes and their teeth. Four large submedian labial papillae situated at base of pseudolabia (near their margins) and pair of lateral amphids present. Two marked, rather wide lateral bands of hypodermal cells, resembling bacillary bands in trichuroids, extending along whole body. Oesophagus muscular, appearing to be formed by two layers; its posterior half distinctly broader than anterior part; anterior end of oesophagus somewhat widened in dorsoventral view (®gure 3D). Posterior end of oesophagus opening into small transverse ventriculus-like formation showing two-layered structure, like that of oesophagus; this formation slightly broader than oesophagus. Ventriculus-like formation opening into intestine through distinct valve. Nerve ring encircling oesophagus approximately at border of its ®rst and second thirds. Excretory pore and small, simple deirids at about same level, somewhat posterior to level of nerve ring. Intestine straight, almost black (containing numerous black granulae), being brown only near its anterior end. Tail of both sexes conical, its tip truncated. Sexual organs concentrated in short section of posterior part of body.

Male (®ve specimens). Length of body 23,196±31,848, maximum width 309±618. Length of pseudolabia 26±52, their width 68±80. Width of lateral hypodermal bands at oesophagus level 113. Oesophagus 1670 ±2036 long (6.1±8.0% of body length), maximum width 174±218. Nerve ring and excretory pore 661±713 and 896±940, respectively, from anterior extremity. Deirids 892±1035 from anterior end of body. Ventriculus-like formation 80±96 long and 176±235 wide. Anterior end of testis far from oesophagus end. Cloacal region of body with short, narrow subventral caudal alae, extending posteriorly approximately to middle of tail. Preanal papillae: three pairs of large, equally spaced subventral papillae, of which last pair at region of caudal alae; one pair of small ventral papillae approximately at level of last pair of subventrals, and one large unpaired median papilla situated somewhat anterior to level of ventral papillae, at level of beginning of caudal alae. Adanal papillae: one pair of small subventral papillae supporting caudal alae. Postanal papillae: one pair of small ventral papillae and three pairs of subventral papillae situated at anterior half of tail, in region of caudal alae; papillae of last but one pair of subventrals rather large, situated more ventrally than two pairs of subventrals; papillae of ®rst, second and fourth pairs of postanal papillae small. Pair of small lateral phasmids present near end of caudal alae. Ventral precloacal region with numerous subventral oblique muscle bands; precloacal sucker absent. Spicules equal, alate, 1523±1766 long, with somewhat widened and almost pointed tip, forming 5.0±6.6% of body length. Weakly sclerotized gubernaculum 128±152 long present. Tail 383±470 long.

Female (®ve gravid specimens). Length of body 28,634±33,578, maximum width 865±1133. Length of pseudolabia 40±60, their width 80±140. Width of lateral hypodermal bands at oesophagu s level 122±148. Oesophagu s 1644±2288 long (5.5±7.9% of body length), maximum width 183±270. Nerve ring and excretory pore 696±713 and 844±974, respectively, from anterior extremity. Deirids 832±1035 from anterior end of body. Ventriculus-like formation 78±100 long and 188±270 wide. Vulva postequatorial, 8219±12,154 from posterior extremity (at 60±72% of body length); vulval lips somewhat sclerotized, not elevated. Muscular vagina directed ®rst posteriorly and then anteriorly from vulva. Amphidelphic. Body at region of vulva conspicuously distended. Eggs numerous, but only few mature eggs present at its distal part. Mature eggs oval, thin-walled, non-embryonated, size 112±148Ö84±100. Anterior ovary far posterior to oesophagus end. Tail 539±626 long.

Host. Deep-water catshark, Apristurus fedorovi Dolganov, Japanese name`arameherazame ’ ( Scyliorhinidae , Carcharhiniformes ).

Site of infection. Intestine.

L ocality. O Iwate and Aomori Prefectures , northern Honshu , Japan, North Paci ®c Ocean (depth 1290±1300 m) (11± 25 September 1978) .

Intensity of infection: three sharks contained two, three and 23 nematode specimens.

Comments

Machida et al. (1982) described a new nematode genus and species, Metaleptus rabuka Machida, Ogawa and Okiyama, 1982 from the stomach and intestine of the deep-sea frill shark, Chlamydoselachus anguiuneus Garman , caught o the Paci®c coast of central Honshu, Japan. The authors assigned Metaleptus Machida, Ogawa and Okiyama, 1982 to the family Physalopteridae , subfamily Proleptinae , of the order Spirurida . Nematodes of this genus have not been recorded since.

In spite of the fact that the original description of M. rabuka is rather brief and the authors did not study the male caudal end in ventral view to ®nd the exact number and arrangement of caudal papillae, nematodes of the present material show practically the same morphology and measurements and we consider them to be M. rabuka ; this is supported by the fact that both forms were recorded from deepsea sharks of the same region.

In contrast to our ®ndings, Machida et al. (1982) reported only four pairs of preanal and four pairs of postanal papillae on the male caudal end of M. rabuka , observed in lateral view. However, an examination in ventral view shows the presence of an additional, rather large unpaired median preanal papilla, one pair of small subventral adanal papillae, four pairs of postanal papillae, and the presence of a pair of minute lateral phasmids. The presence of a gubernaculum and subventral precloacal oblique muscle bands were not mentioned in the original description. Machida et al. (1982) described the inner surface of each labium to bear`three bi- or trifurcate teeth’, but the SEM examination shows that each labium is always provided with three lobes bearing three apical teeth formed by three sclerotized pieces, one larger in the middle and one smaller on either side (®gure 5C, D).

A remarkable feature of M. rabuka is the structure of the oesophagus and the presence of a ventriculus-like formation between the oesophagus and intestine, which is unique amongst all Spirurida . Machida et al. (1982) described the latter as`oesophagus connected with intestine at a short interval where well-developed oesophagointestinal valve inserted’. In fact, the tissue of this peculiar organ is somewhat di erent from that of the oesophagus, although it appears to have a two-layered structure like the oesophagus, and it opens into the intestine through a distinct valve. Since M. rabuka exhibits undoubtedly primitive characters, showing a nities to several higher taxonomic groups, and because it is the parasite of primitive hosts (sharks), it may well be that this ventriculus-like formation gradually evolved into a true ventriculus in ancient ascaridoids.

It has been mentioned above that Machida et al. (1982) assigned M. rabuka to the subfamily Proleptinae of the family Physalopteridae . However, even though M. rabuka may be considered a member of the Spirurida in accordance with Chabaud (1974), it exhibits some characters, particularly the presence of trilobed pseudolabia, which are in a contradiction with the diagnosis of the superfamily Physalopteroide a (see Skryabin and Sobolev, 1964; Chabaud, 1974). In contrast to the morphology of M. rabuka , the oesophagus of most physalopteroids is separated into an anterior muscular and a posterior glandular part; they usually possess a cuticular collarette posterior to the pseudolabia, their spicules are mostly unequal, a gubernaculum is absent, and the structure of the male caudal end is di erent (e.g. they have special ventral cuticular ornamentations). In the structure of the eggs (thin-walled shell and non-embryonated content when laid), M. rabuka conspicuously di ers from all species of the Spirurida , with the exception of the Gnathostomatoide a (see Ivashkin and Khromova, 1976).

Although some morphological features found in Metaleptus , particularly the presence of a ventriculus-like formation and ventral precloacal muscle bands in the male, have not been reported for any species of the Gnathostomatoidea , with the only family Gnathostomatidae , we consider it reasonable to transfer Metaleptus from Physalopteroidea to Gnathostomatoidea . A characteristic feature of most gnathostomatoi d nematodes, i.e. the presence of four to six unicellular, sac-like oesophageal glands, is absent in Metaleptus , as well as in the gnathostomati d subfamily Spiroxyinae . Metaleptus di ers conspicuously from members of the latter subfamily in having a ventriculus-like formation, pseudolabia with reduced lobes, and in a di erent structure to the male caudal end.

In our opinion, the morphology of Metaleptus is so di erent from that of other gnathostomatids that we consider it necessary to create a new subfamily to accommodate it.